HIV-1 prophylactic vaccine comprised of topical DermaVir prime and protein boost elicits cellular immune responses and controls pathogenic R5 SHIV162P3

Virology

Volumn 366, Issue 1, 2007, Pages 197-211

  Cristillo, Anthony D ^a   Lisziewicz, Julianna ^b   He, Leilei ^a   Lori, Franco ^c   Galmin, Lindsey ^a   Trocio, Jeffrey N ^b   Unangst, Tami ^a   Whitman, Lucia ^b   Hudacik, Lauren ^a   Bakare, Nyasha ^b   Whitney, Stephen ^a   Restrepo, Susana ^a   Suschak, John ^a   Grazi Ferrari, Maria ^a   Chung, H K ^a   Kalyanaraman, Vaniambadi S ^a   Markham, Phillip ^a   Pal, Ranajit ^a  

^a ADVANCED BIOSCIENCE LABORATORIES INC   (United States)

^b Genetic Immunity   (United States)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

AIDS; Cellular immune response; HIV 1; T cell memory; Vaccine

Indexed keywords

DERMAVIR; DNA VACCINE; ENVELOPE PROTEIN; GAG PROTEIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COLON; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNIZATION; JEJUNUM; MEMORY T LYMPHOCYTE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; RHESUS MONKEY; TH1 CELL; TH2 CELL; VIREMIA; VIRUS STRAIN;

ACQUIRED IMMUNODEFICIENCY SYNDROME; AIDS VACCINES; ANIMALS; CODON; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GENES, ENV; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNIZATION, SECONDARY; MACACA MULATTA; MICE; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS; TH2 CELLS;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; MUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 34548182353     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.04.012     Document Type: Article

References (77)

1. Ahlers J.D., Belyakov I.M., Thomas E.K., and Berzofsky J.A. High-affinity T helper epitope induces complementary helper and APC polarization, increased CTL, and protection against viral infection. J. Clin. Invest. 108 11 (2001) 1677-1685
2. Allen T.M., Vogel T.U., Fuller D.H., Mothe B.R., Steffen S., Boyson J.E., Shipley T., Fuller J., Hanke T., Sette A., Altman J.D., Moss B., McMichael A.J., and Watkins D.I. Induction of AIDS virus-specific CTL activity in fresh, unstimulated peripheral blood lymphocytes from rhesus macaques vaccinated with a DNA prime/modified vaccinia virus Ankara boost regimen. J. Immunol. 164 9 (2000) 4968-4978
3. Amara R.R., Villinger F., Altman J.D., Lydy S.L., O'Neil S.P., Staprans S.I., Montefiori D.C., Xu Y., Herndon J.G., Wyatt L.S., Candido M.A., Kozyr N.L., Earl P.L., Smith J.M., Ma H.L., Grimm B.D., Hulsey M.L., Miller J., McClure H.M., McNicholl J.M., Moss B., and Robinson H.L. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292 5514 (2001) 69-74
4. Barnett S.W., Rajasekar S., Legg H., Doe B., Fuller D.H., Haynes J.R., Walker C.M., and Steimer K.S. Vaccination with HIV-1 gp120 DNA induces immune responses that are boosted by a recombinant gp120 protein subunit. Vaccine 15 8 (1997) 869-873
5. Barouch D.H., and Letvin N.L. DNA vaccination for HIV-1 and SIV. Intervirology 43 4-6 (2000) 282-287
6. Belyakov I.M., Hammond S.A., Ahlers J.D., Glenn G.M., and Berzofsky J.A. Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J. Clin. Invest. 113 7 (2004) 998-1007
7. + T-cell response in HIV infection. AIDS Rev. 6 2 (2004) 79-88
8. Bevan M.J. Helping the CD8(+) T-cell response. Nat. Rev., Immunol. 4 8 (2004) 595-602
9. Billaut-Mulot O., Idziorek T., Ban E., Kremer L., Dupre L., Loyens M., Riveau G., Locht C., Capron A., and Bahr G.M. Interleukin-18 modulates immune responses induced by HIV-1 Nef DNA prime/protein boost vaccine. Vaccine 19 1 (2000) 95-102
10. Bolesta E., Kowalczyk A., Wierzbicki A., Eppolito C., Kaneko Y., Takiguchi M., Stamatatos L., Shrikant P.A., and Kozbor D. Increased level and longevity of protective immune responses induced by DNA vaccine expressing the HIV-1 Env glycoprotein when combined with IL-21 and IL-15 gene delivery. J. Immunol. 177 1 (2006) 177-191
11. Boyer J.D., Robinson T.M., Kutzler M.A., Parkinson R., Calarota S.A., Sidhu M.K., Muthumani K., Lewis M., Pavlakis G., Felber B., and Weiner D. SIV DNA vaccine co-administered with IL-12 expression plasmid enhances CD8 SIV cellular immune responses in cynomolgus macaques. J. Med. Primatol. 34 5-6 (2005) 262-270
12. Buge S.L., Ma H.L., Amara R.R., Wyatt L.S., Earl P.L., Villinger F., Montefiori D.C., Staprans S.I., Xu Y., Carter E., O'Neil S.P., Herndon J.G., Hill E., Moss B., Robinson H.L., and McNicholl J.M. Gp120-alum boosting of a Gag-Pol-Env DNA/MVA AIDS vaccine: poorer control of a pathogenic viral challenge. AIDS Res. Hum. Retroviruses 19 10 (2003) 891-900
13. Cristillo A.D., Wang S., Caskey M.S., Unangst T., Hocker L., He L., Hudacik L., Whitney S., Keen T., Chou T.H., Shen S., Joshi S., Kalyanaraman V.S., Nair B., Markham P., Lu S., and Pal R. Preclinical evaluation of cellular immune responses elicited by a polyvalent DNA prime/protein boost HIV-1 vaccine. Virology 346 1 (2006) 151-168
14. Dumais N., Patrick A., Moss R.B., Davis H.L., and Rosenthal K.L. Mucosal immunization with inactivated human immunodeficiency virus plus CpG oligodeoxynucleotides induces genital immune responses and protection against intravaginal challenge. J. Infect. Dis. 186 8 (2002) 1098-1105
15. Earl P.L., Sugiura W., Montefiori D.C., Broder C.C., Lee S.A., Wild C., Lifson J., and Moss B. Immunogenicity and protective efficacy of oligomeric human immunodeficiency virus type 1 gp140. J. Virol. 75 2 (2001) 645-653
16. Earl P.L., Wyatt L.S., Montefiori D.C., Bilska M., Woodward R., Markham P.D., Malley J.D., Vogel T.U., Allen T.M., Watkins D.I., Miller N., and Moss B. Comparison of vaccine strategies using recombinant env-gag-pol MVA with or without an oligomeric Env protein boost in the SHIV rhesus macaque model. Virology 294 2 (2002) 270-281
17. Estcourt M.J., McMichael A.J., and Hanke T. DNA vaccines against human immunodeficiency virus type 1. Immunol. Rev. 199 (2004) 144-155
18. Franchini G., Gurunathan S., Baglyos L., Plotkin S., and Tartaglia J. Poxvirus-based vaccine candidates for HIV: two decades of experience with special emphasis on canarypox vectors. Expert Rev. Vaccines 3 4 Suppl. (2004) S75-S88
19. Gherardi M.M., Najera J.L., Perez-Jimenez E., Guerra S., Garcia-Sastre A., and Esteban M. Prime-boost immunization schedules based on influenza virus and vaccinia virus vectors potentiate cellular immune responses against human immunodeficiency virus Env protein systemically and in the genitorectal draining lymph nodes. J. Virol. 77 12 (2003) 7048-7057
20. + T cell immune response against a V3 loop multi-epitope polypeptide (TAB13) of HIV-1 Env after priming with purified fusion protein and booster with modified vaccinia virus Ankara (MVA-TAB) recombinant: a comparison of humoral and cellular immune responses with the vaccinia virus Western Reserve (WR) vector. Vaccine 20 5-6 (2001) 961-971
21. Gomez-Roman V.R., and Robert-Guroff M. Adenoviruses as vectors for HIV vaccines. AIDS Rev. 5 3 (2003) 178-185
22. Gruters R.A., van Baalen C.A., and Osterhaus A.D. The advantage of early recognition of HIV-infected cells by cytotoxic T-lymphocytes. Vaccine 20 15 (2002) 2011-2015
23. Hanke T., McMichael A.J., Mwau M., Wee E.G., Ceberej I., Patel S., Sutton J., Tomlinson M., and Samuel R.V. Development of a DNA-MVA/HIVA vaccine for Kenya. Vaccine 20 15 (2002) 1995-1998
24. Harouse J.M., Gettie A., Eshetu T., Tan R.C., Bohm R., Blanchard J., Baskin G., and Cheng-Mayer C. Mucosal transmission and induction of simian AIDS by CCR5-specific simian/human immunodeficiency virus SHIV(SF162P3). J. Virol. 75 4 (2001) 1990-1995
25. Horner A.A., Datta S.K., Takabayashi K., Belyakov I.M., Hayashi T., Cinman N., Nguyen M.D., Van Uden J.H., Berzofsky J.A., Richman D.D., and Raz E. Immunostimulatory DNA-based vaccines elicit multifaceted immune responses against HIV at systemic and mucosal sites. J. Immunol. 167 3 (2001) 1584-1591
26. Jiang W., Jin N., Cui S., Li Z., Zhang L., Wang H., and Han W. Enhancing immune responses against HIV-1 DNA vaccine by coinoculating IL-6 expression vector. J. Virol. Methods 136 1-2 (2006) 1-7
27. Klenerman P., Phillips R.E., Rinaldo C.R., Wahl L.M., Ogg G., May R.M., McMichael A.J., and Nowak M.A. Cytotoxic T lymphocytes and viral turnover in HIV type 1 infection. Proc. Natl. Acad. Sci. U.S.A. 93 26 (1996) 15323-15328
28. Kojima Y., Xin K.Q., Ooki T., Hamajima K., Oikawa T., Shinoda K., Ozaki T., Hoshino Y., Jounai N., Nakazawa M., Klinman D., and Okuda K. Adjuvant effect of multi-CpG motifs on an HIV-1 DNA vaccine. Vaccine 20 23-24 (2002) 2857-2865
29. Kong W.P., Huang Y., Yang Z.Y., Chakrabarti B.K., Moodie Z., and Nabel G.J. Immunogenicity of multiple gene and clade human immunodeficiency virus type 1 DNA vaccines. J. Virol. 77 23 (2003) 12764-12772
30. Kutzler M.A., Robinson T.M., Chattergoon M.A., Choo D.K., Choo A.Y., Choe P.Y., Ramanathan M.P., Parkinson R., Kudchodkar S., Tamura Y., Sidhu M., Roopchand V., Kim J.J., Pavlakis G.N., Felber B.K., Waldmann T.A., Boyer J.D., and Weiner D.B. Coimmunization with an optimized IL-15 plasmid results in enhanced function and longevity of CD8 T cells that are partially independent of CD4 T cell help. J. Immunol. 175 1 (2005) 112-123
31. Letvin N.L., Montefiori D.C., Yasutomi Y., Perry H.C., Davies M.E., Lekutis C., Alroy M., Freed D.C., Lord C.I., Handt L.K., Liu M.A., and Shiver J.W. Potent, protective anti-HIV immune responses generated by bimodal HIV envelope DNA plus protein vaccination. Proc. Natl. Acad. Sci. U.S.A. 94 17 (1997) 9378-9383
32. + central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312 5779 (2006) 1530-1533
33. Lichterfeld M., Yu X.G., Waring M.T., Mui S.K., Johnston M.N., Cohen D., Addo M.M., Zaunders J., Alter G., Pae E., Strick D., Allen T.M., Rosenberg E.S., Walker B.D., and Altfeld M. HIV-1-specific cytotoxicity is preferentially mediated by a subset of CD8(+) T cells producing both interferon-gamma and tumor necrosis factor-alpha. Blood 104 2 (2004) 487-494
34. Lisziewicz J., Gabrilovich D.I., Varga G., Xu J., Greenberg P.D., Arya S.K., Bosch M., Behr J.P., and Lori F. Induction of potent human immunodeficiency virus type 1-specific T-cell-restricted immunity by genetically modified dendritic cells. J. Virol. 75 16 (2001) 7621-7628
35. Lisziewicz J., Bakare N., and Lori F. Therapeutic vaccination for future management of HIV/AIDS. Vaccine 21 7-8 (2003) 620-623
36. Lisziewicz J., Trocio J., Whitman L., Varga G., Xu J., Bakare N., Erbacher P., Fox C., Woodward R., Markham P., Arya S., Behr J.P., and Lori F. DermaVir: a novel topical vaccine for HIV/AIDS. J. Invest. Dermatol. 124 1 (2005) 160-169
37. Lisziewicz J., Trocio J., Xu J., Whitman L., Ryder A., Bakare N., Lewis M.G., Wagner W., Pistorio A., Arya S., and Lori F. Control of viral rebound through therapeutic immunization with DermaVir. Aids 19 1 (2005) 35-43
38. Lisziewicz J., Kelly L., and Lori F. Topical DermaVir vaccine targeting dendritic cells. Curr. Drug Deliv. 3 1 (2006) 83-88
39. Liu L.J., Watabe S., Yang J., Hamajima K., Ishii N., Hagiwara E., Onari K., Xin K.Q., and Okuda K. Topical application of HIV DNA vaccine with cytokine-expression plasmids induces strong antigen-specific immune responses. Vaccine 20 1-2 (2001) 42-48
40. Liu L., Chahroudi A., Silvestri G., Wernett M.E., Kaiser W.J., Safrit J.T., Komoriya A., Altman J.D., Packard B.Z., and Feinberg M.B. Visualization and quantification of T cell-mediated cytotoxicity using cell-permeable fluorogenic caspase substrates. Nat. Med. 8 2 (2002) 185-189
41. Liu L., Packard B.Z., Brown M.J., Komoriya A., and Feinberg M.B. Assessment of lymphocyte-mediated cytotoxicity using flow cytometry. Methods Mol. Biol. 263 (2004) 125-140
42. Lori F., Trocio J., Bakare N., Kelly L.M., and Lisziewicz J. DermaVir, a novel HIV immunisation technology. Vaccine 23 17-18 (2005) 2030-2034
43. Lu, S. (2003). Immunogenicity and neutralizing antibody responses induced by monovalent and polyvalent DNA prime + protein boost formulations encoding primary HIV-1 Env antigens.
44. Mattapallil J.J., Douek D.C., Buckler-White A., Montefiori D., Letvin N.L., Nabel G.J., and Roederer M. Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. J. Exp. Med. 203 6 (2006) 1533-1541
45. Moss R.B., Diveley J., Jensen F., and Carlo D.J. In vitro immune function after vaccination with an inactivated, gp120-depleted HIV-1 antigen with immunostimulatory oligodeoxynucleotides. Vaccine 18 11-12 (2000) 1081-1087
46. O'Neill E., Martinez I., Villinger F., Rivera M., Gascot S., Colon C., Arana T., Sidhu M., Stout R., Montefiori D.C., Martinez M., Ansari A.A., Israel Z.R., and Kraiselburd E. Protection by SIV VLP DNA prime/protein boost following mucosal SIV challenge is markedly enhanced by IL-12/GM-CSF co-administration. J. Med. Primatol. 31 4-5 (2002) 217-227
47. Otero M., Calarota S.A., Felber B., Laddy D., Pavlakis G., Boyer J.D., and Weiner D.B. Resiquimod is a modest adjuvant for HIV-1 gag-based genetic immunization in a mouse model. Vaccine 22 13-14 (2004) 1782-1790
48. Ozaki T., Yauchi M., Xin K.Q., Hirahara F., and Okuda K. Cross-reactive protection against influenza A virus by a topically applied DNA vaccine encoding M gene with adjuvant. Viral Immunol. 18 2 (2005) 373-380
49. Pal R., Venzon D., Letvin N.L., Santra S., Montefiori D.C., Miller N.R., Tryniszewska E., Lewis M.G., VanCott T.C., Hirsch V., Woodward R., Gibson A., Grace M., Dobratz E., Markham P.D., Hel Z., Nacsa J., Klein M., Tartaglia J., and Franchini G. ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J. Virol. 76 1 (2002) 292-302
50. Pal R., Wang S., Kalyanaraman V.S., Nair B.C., Cristillo A.D., Whitney S., Keen T., Hocker L., Hudacik L., Rose N., Yu Q., Mboudjeka I., Shen S., Chou T., Montefiori D., Mascola J., Markham P., and Lu S. Preclinical immunogenicity and toxicity evaluation of a polyvalent DNA prime/protein boost HIV-1 vaccine. The XV International AIDS Conference Bankok, Thailand (2004)
51. Pal R., Wang S., Kalyanaraman V.S., Nair B.C., Whitney S., Keen T., Hocker L., Hudacik L., Rose N., Cristillo A., Mboudjeka I., Shen S., Wu-Chou T.H., Montefiori D., Mascola J., Lu S., and Markham P. Polyvalent DNA prime and envelope protein boost HIV-1 vaccine elicits humoral and cellular responses and controls plasma viremia in rhesus macaques following rectal challenge with an R5 SHIV isolate. J. Med. Primatol. 34 5-6 (2005) 226-236
52. Pal R., Kalyanaraman V.S., Nair B.C., Whitney S., Keen T., Hocker L., Hudacik L., Rose N., Mboudjeka I., Shen S., Wu-Chou T.H., Montefiori D., Mascola J., Markham P., and Lu S. Immunization of rhesus macaques with a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 vaccine elicits protective antibody response against simian human immunodeficiency virus of R5 phenotype. Virology 348 2 (2006) 341-353
53. + T cell loss and reduces systemic and mucosal SHIVKU2 RNA levels. J. Virol. 80 (2006) 3732-3740
54. Pal R., Yu Q., Wang S., Kalyanaraman V.S., Nair B.C., Hudacik L., Whitney S., Keen T., Hung C.L., Hocker L., Kennedy J.S., Markham P.D., and Lu S. Definitive toxicology and biodistribution study of a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 (HIV-1) vaccine in rabbits. Vaccine 24 (2006) 1225-1234
55. Pantaleo G., and Fauci A.S. Immunopathogenesis of HIV infection. Annu. Rev. Microbiol. 50 (1996) 825-854
56. Partidos C.D., Moreau E., Chaloin O., Tunis M., Briand J.P., Desgranges C., and Muller S. A synthetic HIV-1 Tat protein breaches the skin barrier and elicits Tat-neutralizing antibodies and cellular immunity. Eur. J. Immunol. 34 12 (2004) 3723-3731
57. Peng B., Voltan R., Cristillo A.D., Alvord W.G., Davis-Warren A., Zhou Q., Murthy K.K., and Robert-Guroff M. Replicating Ad-recombinants encoding non-myristoylated rather than wild-type HIV Nef elicit enhanced cellular immunity. Aids 20 17 (2006) 2149-2157
58. Rasmussen R.A., Hofmann-Lehman R., Montefiori D.C., Li P.L., Liska V., Vlasak J., Baba T.W., Schmitz J.E., Kuroda M.J., Robinson H.L., McClure H.M., Lu S., Hu S.L., Rizvi T.A., and Ruprecht R.M. DNA prime/protein boost vaccine strategy in neonatal macaques against simian human immunodeficiency virus. J. Med. Primatol. 31 1 (2002) 40-60
59. Reyes-Sandoval A., Fitzgerald J.C., Grant R., Roy S., Xiang Z.Q., Li Y., Gao G.P., Wilson J.M., and Ertl H.C. Human immunodeficiency virus type 1-specific immune responses in primates upon sequential immunization with adenoviral vaccine carriers of human and simian serotypes. J. Virol. 78 14 (2004) 7392-7399
60. Romano J.W., Shurtliff R.N., Dobratz E., Gibson A., Hickman K., Markham P.D., and Pal R. Quantitative evaluation of simian immunodeficiency virus infection using NASBA technology. J. Virol. Methods 86 1 (2000) 61-70
61. Rose N.F., Marx P.A., Luckay A., Nixon D.F., Moretto W.J., Donahoe S.M., Montefiori D., Roberts A., Buonocore L., and Rose J.K. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106 5 (2001) 539-549
62. Santra S., Barouch D.H., Korioth-Schmitz B., Lord C.I., Krivulka G.R., Yu F., Beddall M.H., Gorgone D.A., Lifton M.A., Miura A., Philippon V., Manson K., Markham P.D., Parrish J., Kuroda M.J., Schmitz J.E., Gelman R.S., Shiver J.W., Montefiori D.C., Panicali D., and Letvin N.L. Recombinant poxvirus boosting of DNA-primed rhesus monkeys augments peak but not memory T lymphocyte responses. Proc. Natl. Acad. Sci. U.S.A. 101 30 (2004) 11088-11093
63. Sharpe S., Hanke T., Tinsley-Bown A., Dennis M., Dowall S., McMichael A., and Cranage M. Mucosal immunization with PLGA-microencapsulated DNA primes a SIV-specific CTL response revealed by boosting with cognate recombinant modified vaccinia virus Ankara. Virology 313 1 (2003) 13-21
64. Shiver J.W., Fu T.M., Chen L., Casimiro D.R., Davies M.E., Evans R.K., Zhang Z.Q., Simon A.J., Trigona W.L., Dubey S.A., Huang L., Harris V.A., Long R.S., Liang X., Handt L., Schleif W.A., Zhu L., Freed D.C., Persaud N.V., Guan L., Punt K.S., Tang A., Chen M., Wilson K.A., Collins K.B., Heidecker G.J., Fernandez V.R., Perry H.C., Joyce J.G., Grimm K.M., Cook J.C., Keller P.M., Kresock D.S., Mach H., Troutman R.D., Isopi L.A., Williams D.M., Xu Z., Bohannon K.E., Volkin D.B., Montefiori D.C., Miura A., Krivulka G.R., Lifton M.A., Kuroda M.J., Schmitz J.E., Letvin N.L., Caulfield M.J., Bett A.J., Youil R., Kaslow D.C., and Emini E.A. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415 6869 (2002) 331-335
65. Skountzou I., Quan F.S., Jacob J., Compans R.W., and Kang S.M. Transcutaneous immunization with inactivated influenza virus induces protective immune responses. Vaccine 24 35-36 (2006) 6110-6119
66. Soudeyns H., and Pantaleo G. The moving target: mechanisms of HIV persistence during primary infection. Immunol. Today 20 10 (1999) 446-450
67. + T lymphocytes both contribute to immunity to adenovirus serotype 5 vaccine vectors. J. Virol. 78 6 (2004) 2666-2673
68. + T cells after acute infection. Nat. Immunol. 5 9 (2004) 927-933
69. Tritel M., Stoddard A.M., Flynn B.J., Darrah P.A., Wu C.Y., Wille U., Shah J.A., Huang Y., Xu L., Betts M.R., Nabel G.J., and Seder R.A. Prime-boost vaccination with HIV-1 Gag protein and cytosine phosphate guanosine oligodeoxynucleotide, followed by adenovirus, induces sustained and robust humoral and cellular immune responses. J. Immunol. 171 5 (2003) 2538-2547
70. + central memory T cells in protection from simian AIDS. J. Immunol. 175 6 (2005) 3502-3507
71. Wagner R., Shao Y., and Wolf H. Correlates of protection, antigen delivery and molecular epidemiology: basics for designing an HIV vaccine. Vaccine 17 13-14 (1999) 1706-1710
72. Wang S., Arthos J., Lawrence J.M., Van Ryk D., Mboudjeka I., Shen S., Chou T.H., Montefiori D.C., and Lu S. Enhanced immunogenicity of gp120 protein when combined with recombinant DNA priming to generate antibodies that neutralize the JR-FL primary isolate of human immunodeficiency virus type 1. J. Virol. 79 12 (2005) 7933-7937
73. Wee E.G., Patel S., McMichael A.J., and Hanke T. A DNA/MVA-based candidate human immunodeficiency virus vaccine for Kenya induces multi-specific T cell responses in rhesus macaques. J. Gen. Virol. 83 Pt. 1 (2002) 75-80
74. + T cell responses in nonhuman primates. Proc. Natl. Acad. Sci. U.S.A. 102 42 (2005) 15190-15194
75. Woodberry T., Gardner J., Elliott S.L., Leyrer S., Purdie D.M., Chaplin P., and Suhrbier A. Prime boost vaccination strategies: CD8 T cell numbers, protection, and Th1 bias. J. Immunol. 170 5 (2003) 2599-2604
76. + T-cell responses following acute HIV-1 infection. J. Virol. 76 17 (2002) 8690-8701
77. Zhao J., Lou Y., Pinczewski J., Malkevitch N., Aldrich K., Kalyanaraman V.S., Venzon D., Peng B., Patterson L.J., Edghill-Smith Y., Woodward R., Pavlakis G.N., and Robert-Guroff M. Boosting of SIV-specific immune responses in rhesus macaques by repeated administration of Ad5hr-SIVenv/rev and Ad5hr-SIVgag recombinants. Vaccine 21 25-26 (2003) 4022-4035